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Molecular Regulation and Disruption of the Progesterone Receptor Signaling Pathways During Frog Embryonic Development

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Molecular Regulation and Disruption of the Progesterone Receptor Signaling Pathways During Frog Embryonic Development MOLECULAR REGULATION AND DISRUPTION OF THE PROGESTERONE RECEPTOR SIGNALING PATHWAYS DURING FROG EMBRYONIC DEVELOPMENT by Paisley Elizabeth Thomson A thesis submitted to the School of Environmental Studies In conformity with the requirements for the degree of Master of Environmental Studies Queen’s University Kingston, Ontario, Canada (May, 2018) Copyright © Paisley Thomson, 2018 Abstract Gestagens are a class of steroid hormones capable of binding and activating progesterone receptors. Gestagens include endogenous progestogens, such as progesterone (P4), which have critically important roles in vertebrate physiology and reproduction and synthetic P4 analogues (progestins), such as melengestrol acetate (MGA). Both gestagens are administered as growth promotants in beef cattle and have been measured in surface water receiving runoff from animal agricultural operations. This project aims to understand the roles and the regulatory mechanisms of P4 in early amphibian development and to assess the consequences of exposures to environmental gestagens on the P4-receptor signaling pathways in frog embryos. We first established the developmental transcript profiles of the three P4 receptors in Western clawed frog (Silurana tropicalis) embryos. P4-receptor mRNAs were detected but differentially expressed throughout embryogenesis. Secondly, we conducted P4 and MGA acute exposures to an environmentally realistic range of concentrations to determine the effects of embryonic exposure to gestagens on development, mortality, and gene expression of reproduction-related genes. Acute exposure to P4 induced a 2- to 5-fold change increase of steroid hormone receptor mRNA levels, whereas MGA exposure induced a dissimilar transcriptional profile than P4. Therefore, we conclude that that MGA and P4 may signal through different molecular cascades in frogs. This is the first study to report developmental transcript profiles in embryonic frogs and to assess the molecular effects of MGA exposure in frogs. While our data suggests that P4 and MGA have dissimilar effects, exposure to either P4 or MGA induced multiple endocrine responses and adverse effects at environmentally realistic concentrations in S. tropicalis. Therefore, we conclude that environmental gestagen contamination may pose a risk to wild populations of amphibians. ii Co-Authorship This thesis is organized according to the manuscript format as outlined in the guidelines provided by the school of Graduate Studies and Research at Queen’s University. All chapters in this thesis are co-authored by Dr. Valerie Langlois (Institut national de la recherche scientifique (INRS), Quebec City, QC, and the School of Environmental Studies, Queen’s University, Kingston, ON). Other significant contributions are recognized in the acknowledgements section of each chapter. iii Acknowledgements Firstly, I would like to express my gratitude to my supervisor, Dr. Valerie Langlois, for the opportunity to pursue a Master’s degree in Environmental studies and work on such an exciting and novel project. Your expertise and support fostered an energy that motivated myself and other members of the lab to thrive. Moreover, the opportunities to publish and attend conferences were immensely beneficial to me as a scientist and I will use what I gained from these experiences going forward. I have learned so much while pursuing this degree and look forward to continuing to develop as a researcher under your mentorship. Thank you to my committee members Dr. Louise Winn and Dr. Eric Dumont for contributing your expertise and providing me with input that aided me greatly in the completion of this thesis. I appreciate your advice! I would like to thank Tyler Rozario and Meghan Hinds who were instrumental in helping with RNA isolation and other molecular lab work for my developmental profiles and gestagen exposures. I am also grateful to Marco Piñeada and Dr. Viviane Yargeau for carrying out the chemical analysis of the media samples from the acute exposures. I also would like to thank Drs. Peter Hodson and Stephen Brown and the members of their lab group. Thank you for the opportunity to learn and share my work with such an enthusiastic and helpful group of researchers. Your feedback was beneficial in many aspects of my thesis, from experimental design, to interpreting data, to presenting my findings. Thank you to current and former members of the Langlois Lab, especially: Dr. Sonja Bissegger, Dr. Lucie Baillon, Dr. Diana Campbell, Chrissy Emerton, Linda Lara, Dr. Barry Madison, and Sarah Wallace. I could not have managed my project without your help! Whether iv it was help in the animal rooms, in the lab, or at meetings, your collaborative spirit was always appreciated! Thank you to my instructors and classmates in the School of Environmental Studies; especially Tash Lynn Colson, Julie Adams, and Kamila Pogoda. Thank you for all the help both inside and outside of class. Your friendship has been a highlight of my experience at Queen’s and was fundamental to my success in this project! To my family - my parents, grandparents, Cameron, and Bryce; thank you so much for your love and encouragement. I am so grateful for the emotional and financial support over the years as I have furthered my education. I hope you know how lucky I feel to have such fantastic role models to look up to. Finally, to Kass. Your love means everything to me! I hope you know how important it was to have your encouragement, comfort, and silliness to help me get through this project. We’ve been alongside each other throughout our Master’s theses and I can’t wait to experience the next chapter of our lives together. v Statement of Originality I hereby certify that the work contained within this thesis is the original work of the authors and has not been previously submitted for a degree or diploma at any other educational institution. Any published (or unpublished) ideas and/or techniques from the work of others are fully acknowledged in accordance with the standard referencing practices. (Paisley Thomson) (April, 2018) vi Table of Contents Abstract ...................................................................................................................................... ii Co-Authorship ........................................................................................................................... iii Acknowledgements ................................................................................................................... iv Statement of Originality ............................................................................................................. vi List of Figures ........................................................................................................................... ix List of Tables .............................................................................................................................. x List of Abbreviations ................................................................................................................. xi Chapter 1 General Introduction and Literature Review ........................................................ 1 1.1 Problem Identification ....................................................................................................... 1 1.2 Literature Review .............................................................................................................. 2 1.2.1 Gestagens: Progestogens ............................................................................................. 2 1.2.2 Mechanism of action ................................................................................................... 6 1.2.3 Progestins ................................................................................................................. 10 1.2.4 Progestin classification and pharmacodynamics ........................................................ 12 1.3 Gestagens as endocrine disrupting chemicals in aquatic vertebrates ................................. 14 1.3.1 Fish early life stages.................................................................................................. 16 Progesterone .................................................................................................................. 16 Progestins ...................................................................................................................... 18 1.3.2 Amphibians .............................................................................................................. 21 Progesterone .................................................................................................................. 21 Progestins ...................................................................................................................... 23 1.4 Western clawed frog (Silurana tropicalis) ....................................................................... 27 1.5 Research aims, hypotheses, and objectives ...................................................................... 28 Chapter 2 Developmental profiles of progesterone receptor transcripts and molecular responses to gestagen exposure during Silurana tropicalis early development .................... 38 2.1 Introduction ..................................................................................................................... 39 2.2 Materials and methods ..................................................................................................... 43 2.2.1 Breeding and
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